OCR-Stats: Robust estimation and statistical testing of mitochondrial respiration activities using Seahorse XF Analyzer

PLoS One. 2018 Jul 11;13(7):e0199938. doi: 10.1371/journal.pone.0199938. eCollection 2018.

Abstract

The accurate quantification of cellular and mitochondrial bioenergetic activity is of great interest in medicine and biology. Mitochondrial stress tests performed with Seahorse Bioscience XF Analyzers allow the estimation of different bioenergetic measures by monitoring the oxygen consumption rates (OCR) of living cells in multi-well plates. However, studies of the statistical best practices for determining aggregated OCR measurements and comparisons have been lacking. Therefore, to understand how OCR behaves across different biological samples, wells, and plates, we performed mitochondrial stress tests in 126 96-well plates involving 203 fibroblast cell lines. We show that the noise of OCR is multiplicative, that outlier data points can concern individual measurements or all measurements of a well, and that the inter-plate variation is greater than the intra-plate variation. Based on these insights, we developed a novel statistical method, OCR-Stats, that: i) robustly estimates OCR levels modeling multiplicative noise and automatically identifying outlier data points and outlier wells; and ii) performs statistical testing between samples, taking into account the different magnitudes of the between- and within-plate variations. This led to a significant reduction of the coefficient of variation across plates of basal respiration by 45% and of maximal respiration by 29%. Moreover, using positive and negative controls, we show that our statistical test outperforms the existing methods, which suffer from an excess of either false positives (within-plate methods), or false negatives (between-plate methods). Altogether, this study provides statistical good practices to support experimentalists in designing, analyzing, testing, and reporting the results of mitochondrial stress tests using this high throughput platform.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • Cell Respiration
  • Energy Metabolism
  • Fibroblasts / cytology
  • Mitochondria / metabolism*
  • Models, Statistical
  • Oxygen Consumption
  • Tissue Array Analysis / methods*

Grants and funding

This study was supported by the German Bundesministerium für Bildung und Forschung (BMBF) through the German Network for mitochondrial disorders (mitoNET, 01GM1113C to HP), the E-Rare project GENOMIT (01GM1207 to HP), the Juniorverbund in der Systemmedizin ‘mitOmics’ (FKZ 01ZX1405A JG, LW and VAY), the DZHK (German Centre for Cardiovascular Research, LSK), the German Research Foundation (DFG) and the Technical University of Munich (TUM) in the framework of the Open Access Publishing Program. A Fellowship through the Graduate School of Quantitative Biosciences Munich (QBM) supports VAY. HP is supported by EU FP7 Mitochondrial European Educational Training Project (317433). JG, VAY, LSK and RK and HP are supported by EU Horizon2020 Collaborative Research Project SOUND (633974). We thank the Cell lines and DNA Bank of Pediatric Movement Disorders and Mitochondrial Diseases of the Telethon Genetic Biobank Network (GTB09003).